The Phylogenetic Limits to Diversity-Dependent Diversification.

While the theory of micro-evolution by natural selection assigns a crucial role to competition, its role in macroevolution is less clear. Phylogenetic evidence for a decelerating accumulation of lineages suggests a feedback of lineage diversity on diversification. However, does this feedback only occur between close relatives, or do distant relatives also influence each other's diversification? In other words: are there phylogenetic limits to this diversity-dependence? Islands form ideal systems to answer these questions because their boundedness facilitates an overview of all potential competitors. The DAISIE (Dynamic Assembly of Island biota through Speciation Immigration and Extinction) framework allows for testing the presence of diversity-dependence on islands given phylogenetic data on colonization and branching times. The current inference models in DAISIE assume that this diversity-dependence only applies within a colonizing clade, i.e., all mainland species can colonize and diversify independently from one another. We term this clade-specific (CS) diversity-dependence. Here we introduce a new DAISIE model that assumes that diversity-dependence applies to all island species of a taxonomic group regardless of their mainland ancestry, i.e., diversity-dependence applies both to species within the same clade and between different clades established by different mainland species. We call this island-wide (IW) diversity-dependence. We present a method to compute a likelihood for this model given phylogenetic data on colonization and branching events and use likelihood ratio bootstrapping to compare it to the likelihood of the CS model in order to overcome biases known for standard model selection. We apply it to the diversification of Eleutherodactylus frogs on Hispaniola. Across the Greater Antilles archipelago, this radiation shows repeated patterns of diversification in ecotypes that are similar across clades. This could be suggestive of overlapping niche space and hence between-clade interactions, i.e., IW diversity-dependence. But it could also be suggestive of only within-clade interactions because between-clade interactions would have blocked the same ecotype from re-appearing. We find that the CS model fits the data much better than the IW model, indicating that different colonizations while resulting in similar ecotypes, are sufficiently distinct to avoid interacting strongly. We argue that non-overlapping distributions between clades (both spatially and in terms of ecotypes) cannot be used as evidence of CS diversity-dependence, because this pattern may be a consequence of IW diversity-dependence. By contrast, by using phylogenetic data rather than distributional data our method does allow for inferring the phylogenetic limits to diversity-dependent diversification. We discuss possibilities for future extensions and applications of our modelling approach. [Adaptive radiation; birth-death model; Caribbean; diversity-dependence; Eleutherodactylus; island biogeography.].

High Investment in Reproduction Is Associated with Reduced Life Span in Dogs.

AbstractProminent differences in aging among and within species present an evolutionary puzzle. The theories proposed to explain evolutionary differences in aging are based on the axiom that selection maximizes fitness, not necessarily life span. This implies trade-offs between investment in self-maintenance and investment in reproduction, where high investments in growth and current reproduction are associated with short life spans. Fast growth and large adult size are related to shorter life spans in the domestic dog, a bourgeoning model in aging research; however, whether reproduction influences life span in this system remains unknown. Here we test the relationship between reproduction and differences in life span among dog breeds, simultaneously controlling for shared ancestry and recent gene flow. We found that shared ancestry explains a higher proportion of the among-breed variation in life history traits, in comparison with recent gene flow. Our results also show that reproductive investment negatively impacts life span, and more strongly so in large breeds, an effect that is not merely a correlated response of adult size. These results suggest that basic life history trade-offs are apparent in a domestic animal whose diversity is the result of artificial selection and that among-breed differences in life span are due to a combination of size and reproduction.

Diversification dynamics in Caribbean rain frogs (Eleutherodactylus) are uncoupled from the anuran community and consistent with adaptive radiation.

Adaptive radiation is proposed to play a key role in generating differences in species richness among lineages and geographical regions. Due to the importance of ecological divergence in adaptive radiation, species richness is predicted to be influenced by equilibrium diversity dynamics, although the concept continues to generate much debate. An additional important question is whether radiating clades have intrinsic biological characteristics that make them particularly prone to diversify. We tackle these questions by analysing (i) the temporal patterns of diversification of Caribbean Eleutherodactylus frogs, and (ii) assembly of the complete native anuran community of the Caribbean archipelago (197 species), testing for the presence of equilibrium dynamics and whether diversification patterns of Eleutherodactylus differ from those of the rest of the Caribbean anurans. Diversification rates follow the predicted pattern of rapid diversification early in the radiation which gradually decreases towards the present. Eleutherodactylus diversification is significantly faster than that of the Caribbean anuran community, and although equilibrium dynamics influence richness of all Caribbean anurans, Eleutherodactylus shows higher carrying capacity. Our results indicate that ecological opportunity per se is not sufficient for adaptive radiation and that diverse lineages present intrinsic characteristics that enable them to make the most of available opportunity.

Evolutionary history of an island endemic, the Azorean common quail.

Oceanic islands are characterized by conditions that favour diversification into endemic lineages that can be very different from their mainland counterparts. This can be the result of fast phenotypic divergence due to drift or the result of slower adaptation to local conditions. This uniqueness can obscure their evolutionary history. Here we used morphological, stable isotope, genetic and genomic data to characterize common quails (Coturnix coturnix) in the Azores archipelago and assess the divergence from neighbouring common quail populations. Historical documents suggested that these quails could have a recent origin associated with the arrival of humans in the last centuries. Our results show that Azorean quails constitute a well-differentiated lineage with small size and dark throat pigmentation that has lost the migratory ability and that diverged from mainland quail lineages more than 0.8 mya, contrary to the notion of a recent human-mediated arrival. Even though some Azorean quails carry an inversion that affects 115 Mbp of chromosome 1 and that has been associated with the loss of the migratory behaviour in other common quail populations, half of the analysed individuals do not have that inversion and still do not migrate. The long coexistence and evolution in isolation in the Azores of two chromosomal variants (with and without the inversion) is best explained by balancing selection. Thus, a unique and long evolutionary history led to the island endemic that we know today, C. c. conturbans.

Large variance in inbreeding within the Iberian wolf population.

The gray wolf (Canis lupus) population on the Iberian Peninsula was the largest in western and central Europe during most of the 20th century, with its size apparently never under a few hundred individuals. After partial legal protection in the 1970s in Spain, the northwest Iberian population increased to about 300-350 packs and then stabilized. In contrast to many current European wolf populations, which have been connected through gene flow, the Iberian wolf population has been isolated for decades. Here we measured changes on genomic diversity and inbreeding through the last decades in a geographic context. We find that the level of genomic diversity in Iberian wolves is low compared to other Eurasian wolf populations. Despite population expansion in the last 50 years, some modern wolves had very high inbreeding, especially in the recently recolonized and historical edge areas. These individuals contrast with others with low inbreeding within the same population. The high variance in inbreeding despite population expansion seems associated with small-scale fragmentation of the range that is revealed by the genetic similarity between modern and historical samples from close localities despite being separated by decades, remaining differentiated from other individuals that are just over 100 km away, a small distance for a species with great dispersal capacity inhabiting a continuous range. This illustrates that, despite its demographically stable condition, the population would probably benefit from favoring connectivity within the population as well as genetic exchange with other European wolf populations to avoid excessive fragmentation and local inbreeding depression.

Phylogenomics and evolutionary history of Oreobates (Anura: Craugastoridae) Neotropical frogs along elevational gradients.

Mountain ranges offer opportunities for understanding how species evolved and diversified across different environmental conditions. Neotropical frogs of the genus Oreobates (Anura: Craugastoridae) are adapted to highland and lowland habitats along the Andes, but many aspects of their evolution remain unknown. We studied their evolutionary history using ~18,000 exons enriched by targeted sequence-capture. Since capture success was very variable across samples, we evaluated to what degree differing data filtering produced robust inferences. The inferred evolutionary framework evidenced phylogenetic discordances among lowland species that can be explained by taxonomic misidentification or admixture of ancestral lineages. Highland species showed smaller effective populations than lowland frogs, probably due to greater habitat fragmentation in montane environments. Stronger genetic drift likely decreased the power of purifying selection and led to an increased proportion of nonsynonymous mutations in highland populations that could play an important role in their adaptation. Overall, our work sheds light on the evolutionary history and diversification of this group of Neotropical frogs along elevational gradients in the Andes as well as on their patterns of intraspecific diversity.

Vastly underestimated species richness of Amazonian salamanders (Plethodontidae: Bolitoglossa) and implications about plethodontid diversification.

We present data showing that the number of salamander species in Amazonia is vastly underestimated. We used DNA sequences of up to five genes (3 mitochondrial and 2 nuclear) of 366 specimens, 189 corresponding to 89 non-Amazonian nominal species and 177 Amazonian specimens, including types or topotypes, of eight of the nine recognized species in the region. By including representatives of all known species of Amazonian Bolitoglossa, except for one, and 73% of the currently 132 recognized species of the genus, our dataset represents the broadest sample of Bolitoglossa species, specimens, and geographic localities studied to date. We performed phylogenetic analyses using parsimony with tree-alignment and maximum likelihood (ML) with similarity alignment, with indels as binary characters. Our optimal topologies were used to delimit lineages that we assigned to nominal species and candidate new species following criteria that maximize the consilience of the current species taxonomy, monophyly, gaps in branch lengths, genetic distances, and geographic distribution. We contrasted the results of our species-delimitation protocol with those of Automated Barcode Gap Discovery (ABGD) and multi-rate Poisson Tree Processes (mPTP). Finally, we inferred the historical biogeography of South American salamanders by dating the trees and using dispersal-vicariance analysis (DIVA). Our results revealed a clade including almost all Amazonian salamanders, with a topology incompatible with just the currently recognized nine species. Following our species-delimitation criteria, we identified 44 putative species in Amazonia. Both ABGD and mPTP inferred more species than currently recognized, but their numbers (23-49) and limits vary. Our biogeographic analysis suggested a stepping-stone colonization of the Amazonian lowlands from Central America through the Chocó and the Andes, with several late dispersals from Amazonia back into the Andes. These biogeographic events are temporally concordant with an early land bridge between Central and South America (~10-15 MYA) and major landscape changes in Amazonia during the late Miocene and Pliocene, such as the drainage of the Pebas system, the establishment of the Amazon River, and the major orogeny of the northern Andes.

Survival and divergence in a small group: The extraordinary genomic history of the endangered Apennine brown bear stragglers.

About 100 km east of Rome, in the central Apennine Mountains, a critically endangered population of ∼50 brown bears live in complete isolation. Mating outside this population is prevented by several 100 km of bear-free territories. We exploited this natural experiment to better understand the gene and genomic consequences of surviving at extremely small population size. We found that brown bear populations in Europe lost connectivity since Neolithic times, when farming communities expanded and forest burning was used for land clearance. In central Italy, this resulted in a 40-fold population decline. The overall genomic impact of this decline included the complete loss of variation in the mitochondrial genome and along long stretches of the nuclear genome. Several private and deleterious amino acid changes were fixed by random drift; predicted effects include energy deficit, muscle weakness, anomalies in cranial and skeletal development, and reduced aggressiveness. Despite this extreme loss of diversity, Apennine bear genomes show nonrandom peaks of high variation, possibly maintained by balancing selection, at genomic regions significantly enriched for genes associated with immune and olfactory systems. Challenging the paradigm of increased extinction risk in small populations, we suggest that random fixation of deleterious alleles (i) can be an important driver of divergence in isolation, (ii) can be tolerated when balancing selection prevents random loss of variation at important genes, and (iii) is followed by or results directly in favorable behavioral changes.

Ecomorphological convergence in Eleutherodactylus frogs: a case of replicate radiations in the Caribbean.

Replicate radiations, the repeated multiplication of species associated with ecological divergence, have attracted much attention and generated as much debate. Due to the few well-studied cases, it remains unclear whether replicate radiations are an exceptional result of evolution or a relatively common example of the power of adaptation by natural selection. We examined the case of Eleutherodactylus frogs, which radiated in the Caribbean islands resulting in more than 160 species that occupy very diverse habitats. A time-calibrated phylogeny revealed that these frogs independently diversified on all larger islands producing species that occupy a broad range of microhabitats in different islands. Using phylogenetic comparative methods, we found an association between morphological traits and particular microhabitats, and for most microhabitats detected significant morphological convergence. Our results indicate Caribbean Eleutherodactylus are a novel example of replicate radiations, and highlight the predictability of evolutionary processes, as similar ecological opportunities can lead to similar outcomes.

Worldwide patterns of genomic variation and admixture in gray wolves.

The gray wolf (Canis lupus) is a widely distributed top predator and ancestor of the domestic dog. To address questions about wolf relationships to each other and dogs, we assembled and analyzed a data set of 34 canine genomes. The divergence between New and Old World wolves is the earliest branching event and is followed by the divergence of Old World wolves and dogs, confirming that the dog was domesticated in the Old World. However, no single wolf population is more closely related to dogs, supporting the hypothesis that dogs were derived from an extinct wolf population. All extant wolves have a surprisingly recent common ancestry and experienced a dramatic population decline beginning at least ∼30 thousand years ago (kya). We suggest this crisis was related to the colonization of Eurasia by modern human hunter-gatherers, who competed with wolves for limited prey but also domesticated them, leading to a compensatory population expansion of dogs. We found extensive admixture between dogs and wolves, with up to 25% of Eurasian wolf genomes showing signs of dog ancestry. Dogs have influenced the recent history of wolves through admixture and vice versa, potentially enhancing adaptation. Simple scenarios of dog domestication are confounded by admixture, and studies that do not take admixture into account with specific demographic models are problematic.

From groups to communities in western lowland gorillas.

Social networks are the result of interactions between individuals at different temporal scales. Thus, sporadic intergroup encounters and individual forays play a central role in defining the dynamics of populations in social species. We assessed the rate of intergroup encounters for three western lowland gorilla ( Gorilla gorilla gorilla) groups with daily observations over 5 years, and non-invasively genotyped a larger population over four months. Both approaches revealed a social system much more dynamic than anticipated, with non-aggressive intergroup encounters that involved social play by immature individuals, exchanges of members between groups likely modulated by kinship, and absence of infanticide evidenced by infants not fathered by the silverback of the group where they were found. This resulted in a community composed of groups that interacted frequently and not-aggressively, contrasting with the more fragmented and aggressive mountain gorilla ( G. beringei beringei) societies. Such extended sociality can promote the sharing of behavioural and cultural traits, but might also increase the susceptibility of western lowland gorillas to infectious diseases that have decimated their populations in recent times.

The genomic basis of adaptation to high-altitude habitats in the eastern honey bee (Apis cerana).

The eastern honey bee (Apis cerana) is of central importance for agriculture in Asia. It has adapted to a wide variety of environmental conditions across its native range in southern and eastern Asia, which includes high-altitude regions. eastern honey bees inhabiting mountains differ morphologically from neighbouring lowland populations and may also exhibit differences in physiology and behaviour. We compared the genomes of 60 eastern honey bees collected from high and low altitudes in Yunnan and Gansu provinces, China, to infer their evolutionary history and to identify candidate genes that may underlie adaptation to high altitude. Using a combination of FST -based statistics, long-range haplotype tests and population branch statistics, we identified several regions of the genome that appear to have been under positive selection. These candidate regions were strongly enriched for coding sequences and had high haplotype homozygosity and increased divergence specifically in highland bee populations, suggesting they have been subjected to recent selection in high-altitude habitats. Candidate loci in these genomic regions included genes related to reproduction and feeding behaviour in honey bees. Functional investigation of these candidate loci is necessary to fully understand the mechanisms of adaptation to high-altitude habitats in the eastern honey bee.

Bottlenecks and selective sweeps during domestication have increased deleterious genetic variation in dogs.

Population bottlenecks, inbreeding, and artificial selection can all, in principle, influence levels of deleterious genetic variation. However, the relative importance of each of these effects on genome-wide patterns of deleterious variation remains controversial. Domestic and wild canids offer a powerful system to address the role of these factors in influencing deleterious variation because their history is dominated by known bottlenecks and intense artificial selection. Here, we assess genome-wide patterns of deleterious variation in 90 whole-genome sequences from breed dogs, village dogs, and gray wolves. We find that the ratio of amino acid changing heterozygosity to silent heterozygosity is higher in dogs than in wolves and, on average, dogs have 2-3% higher genetic load than gray wolves. Multiple lines of evidence indicate this pattern is driven by less efficient natural selection due to bottlenecks associated with domestication and breed formation, rather than recent inbreeding. Further, we find regions of the genome implicated in selective sweeps are enriched for amino acid changing variants and Mendelian disease genes. To our knowledge, these results provide the first quantitative estimates of the increased burden of deleterious variants directly associated with domestication and have important implications for selective breeding programs and the conservation of rare and endangered species. Specifically, they highlight the costs associated with selective breeding and question the practice favoring the breeding of individuals that best fit breed standards. Our results also suggest that maintaining a large population size, rather than just avoiding inbreeding, is a critical factor for preventing the accumulation of deleterious variants.

Demographically-Based Evaluation of Genomic Regions under Selection in Domestic Dogs.

Controlling for background demographic effects is important for accurately identifying loci that have recently undergone positive selection. To date, the effects of demography have not yet been explicitly considered when identifying loci under selection during dog domestication. To investigate positive selection on the dog lineage early in the domestication, we examined patterns of polymorphism in six canid genomes that were previously used to infer a demographic model of dog domestication. Using an inferred demographic model, we computed false discovery rates (FDR) and identified 349 outlier regions consistent with positive selection at a low FDR. The signals in the top 100 regions were frequently centered on candidate genes related to brain function and behavior, including LHFPL3, CADM2, GRIK3, SH3GL2, MBP, PDE7B, NTAN1, and GLRA1. These regions contained significant enrichments in behavioral ontology categories. The 3rd top hit, CCRN4L, plays a major role in lipid metabolism, that is supported by additional metabolism related candidates revealed in our scan, including SCP2D1 and PDXC1. Comparing our method to an empirical outlier approach that does not directly account for demography, we found only modest overlaps between the two methods, with 60% of empirical outliers having no overlap with our demography-based outlier detection approach. Demography-aware approaches have lower-rates of false discovery. Our top candidates for selection, in addition to expanding the set of neurobehavioral candidate genes, include genes related to lipid metabolism, suggesting a dietary target of selection that was important during the period when proto-dogs hunted and fed alongside hunter-gatherers.

On the path to extinction: Inbreeding and admixture in a declining grey wolf population.

Allee effects reduce the viability of small populations in many different ways, which act synergistically to lead populations towards extinction vortexes. The Sierra Morena wolf population, isolated in the south of the Iberian Peninsula and composed of just one or few packs for decades, represents a good example of how diverse threats act additively in very small populations. We sequenced the genome of one of the last wolves identified (and road-killed) in Sierra Morena and that of another wolf in the Iberian Wolf Captive Breeding Program and compared them with other wolf and dog genomes from around the world (including two previously published genome sequences from northern Iberian wolves). The results showed relatively low overall genetic diversity in Iberian wolves, but diverse population histories including past introgression of dog genes. The Sierra Morena wolf had an extraordinarily high level of inbreeding and long runs of homozygosity, resulting from the long isolation. In addition, about one-third of the genome was of dog origin. Despite the introgression of dog genes, heterozygosity remained low because of continued inbreeding after several hybridization events. The results thus illustrate the case of a small and isolated wolf population where the low population density may have favoured hybridization and introgression of dog alleles, but continued inbreeding may have resulted in large chromosomal fragments of wolf origin completely disappearing from the population, and being replaced by chromosomal fragments of dog origin. The latest population surveys suggest that this population may have gone extinct.

Similar genomic proportions of copy number variation within gray wolves and modern dog breeds inferred from whole genome sequencing.

BACKGROUND: Whole genome re-sequencing data from dogs and wolves are now commonly used to study how natural and artificial selection have shaped the patterns of genetic diversity. Single nucleotide polymorphisms, microsatellites and variants in mitochondrial DNA have been interrogated for links to specific phenotypes or signals of domestication. However, copy number variation (CNV), despite its increasingly recognized importance as a contributor to phenotypic diversity, has not been extensively explored in canids. RESULTS: Here, we develop a new accurate probabilistic framework to create fine-scale genomic maps of segmental duplications (SDs), compare patterns of CNV across groups and investigate their role in the evolution of the domestic dog by using information from 34 canine genomes. Our analyses show that duplicated regions are enriched in genes and hence likely possess functional importance. We identify 86 loci with large CNV differences between dogs and wolves, enriched in genes responsible for sensory perception, immune response, metabolic processes, etc. In striking contrast to the observed loss of nucleotide diversity in domestic dogs following the population bottlenecks that occurred during domestication and breed creation, we find a similar proportion of CNV loci in dogs and wolves, suggesting that other dynamics are acting to particularly select for CNVs with potentially functional impacts. CONCLUSIONS: This work is the first comparison of genome wide CNV patterns in domestic and wild canids using whole-genome sequencing data and our findings contribute to study the impact of novel kinds of genetic changes on the evolution of the domestic dog.

Genome sequencing highlights the dynamic early history of dogs.

To identify genetic changes underlying dog domestication and reconstruct their early evolutionary history, we generated high-quality genome sequences from three gray wolves, one from each of the three putative centers of dog domestication, two basal dog lineages (Basenji and Dingo) and a golden jackal as an outgroup. Analysis of these sequences supports a demographic model in which dogs and wolves diverged through a dynamic process involving population bottlenecks in both lineages and post-divergence gene flow. In dogs, the domestication bottleneck involved at least a 16-fold reduction in population size, a much more severe bottleneck than estimated previously. A sharp bottleneck in wolves occurred soon after their divergence from dogs, implying that the pool of diversity from which dogs arose was substantially larger than represented by modern wolf populations. We narrow the plausible range for the date of initial dog domestication to an interval spanning 11-16 thousand years ago, predating the rise of agriculture. In light of this finding, we expand upon previous work regarding the increase in copy number of the amylase gene (AMY2B) in dogs, which is believed to have aided digestion of starch in agricultural refuse. We find standing variation for amylase copy number variation in wolves and little or no copy number increase in the Dingo and Husky lineages. In conjunction with the estimated timing of dog origins, these results provide additional support to archaeological finds, suggesting the earliest dogs arose alongside hunter-gathers rather than agriculturists. Regarding the geographic origin of dogs, we find that, surprisingly, none of the extant wolf lineages from putative domestication centers is more closely related to dogs, and, instead, the sampled wolves form a sister monophyletic clade. This result, in combination with dog-wolf admixture during the process of domestication, suggests that a re-evaluation of past hypotheses regarding dog origins is necessary.

Strong artificial selection in domestic mammals did not result in an increased recombination rate.

Recombination rates vary in intensity and location at the species, individual, sex and chromosome levels. Despite the fundamental biological importance of this process, the selective forces that operate to shape recombination rate and patterns are unclear. Domestication offers a unique opportunity to study the interplay between recombination and selection. In domesticates, intense selection for particular traits is imposed on small populations over many generations, resulting in organisms that differ, sometimes dramatically, in morphology and physiology from their wild ancestor. Although earlier studies suggested increased recombination rate in domesticates, a formal comparison of recombination rates between domestic mammals and their wild congeners was missing. In order to determine broad-scale recombination rate, we used immunolabeling detection of MLH1 foci as crossover markers in spermatocytes in three pairs of closely related wild and domestic species (dog and wolf, goat and ibex, and sheep and mouflon). In the three pairs, and contrary to previous suggestions, our data show that contemporary recombination rate is higher in the wild species. Subsequently, we inferred recombination breakpoints in sequence data for 16 genomic regions in dogs and wolves, each containing a locus associated with a dog phenotype potentially under selection during domestication. No difference in the number and distribution of recombination breakpoints was found between dogs and wolves. We conclude that our data indicate that strong directional selection did not result in changes in recombination in domestic mammals, and that both upper and lower bounds for crossover rates may be tightly regulated.

Fine-scale kin recognition in the absence of social familiarity in the Siberian jay, a monogamous bird species.

Kin recognition is a critical element to kin cooperation, and in vertebrates, it is primarily based on associative learning. Recognition of socially unfamiliar kin occurs rarely, and it is reported only in vertebrate species where promiscuity prevents recognition of first-order relatives. However, it is unknown whether the recognition of socially unfamiliar kin can evolve in monogamous species. Here, we investigate whether genetic relatedness modulates aggression among group members in Siberian jays (Perisoreus infaustus). This bird species is genetically and socially monogamous and lives in groups that are formed through the retention of offspring beyond independence, and the immigration of socially unfamiliar nonbreeders. Observations on feeders showed that genetic relatedness modulated aggression of breeders towards immigrants in a graded manner, in that they chased most intensely the immigrant group members that were genetically the least related. However, cross-fostering experiments showed that breeders were equally tolerant towards their own and cross-fostered young swapped as nestlings. Thus, breeders seem to use different mechanisms to recognize socially unfamiliar individuals and own offspring. As Siberian jays show a high degree of nepotism during foraging and predator encounters, inclusive fitness benefits may play a role for the evolution of fine-scale kin recognition. More generally, our results suggest that fine-graded kin recognition can evolve independently of social familiarity, highlighting the evolutionary importance of kin recognition for social species.

Rethinking dog domestication by integrating genetics, archeology, and biogeography.

The dog was the first domesticated animal but it remains uncertain when the domestication process began and whether it occurred just once or multiple times across the Northern Hemisphere. To ascertain the value of modern genetic data to elucidate the origins of dog domestication, we analyzed 49,024 autosomal SNPs in 1,375 dogs (representing 35 breeds) and 19 wolves. After combining our data with previously published data, we contrasted the genetic signatures of 121 breeds with a worldwide archeological assessment of the earliest dog remains. Correlating the earliest archeological dogs with the geographic locations of 14 so-called "ancient" breeds (defined by their genetic differentiation) resulted in a counterintuitive pattern. First, none of the ancient breeds derive from regions where the oldest archeological remains have been found. Second, three of the ancient breeds (Basenjis, Dingoes, and New Guinea Singing Dogs) come from regions outside the natural range of Canis lupus (the dog's wild ancestor) and where dogs were introduced more than 10,000 y after domestication. These results demonstrate that the unifying characteristic among all genetically distinct so-called ancient breeds is a lack of recent admixture with other breeds likely facilitated by geographic and cultural isolation. Furthermore, these genetically distinct ancient breeds only appear so because of their relative isolation, suggesting that studies of modern breeds have yet to shed light on dog origins. We conclude by assessing the limitations of past studies and how next-generation sequencing of modern and ancient individuals may unravel the history of dog domestication.